Essay
A Unified Classification of Alien Species Based on the
Magnitude of their Environmental Impacts
Tim M. Blackburn1,2,3*, Franz Essl4, Thomas Evans5, Philip E. Hulme6, Jonathan M. Jeschke7,
Ingolf Kühn8,9, Sabrina Kumschick10, Zuzana Marková11,12, Agata Mrugała12, Wolfgang Nentwig13,
Jan Pergl11, Petr Pyšek11,12, Wolfgang Rabitsch14, Anthony Ricciardi15, David M. Richardson10,
Agnieszka Sendek8, Montserrat Vilà16, John R. U. Wilson10,17, Marten Winter9, Piero Genovesi18,
Sven Bacher19
1 Institute of Zoology, Zoological Society of London, London, United Kingdom, 2 Distinguished Scientist Fellowship Program, King Saud University, Riyadh, Saudi Arabia,
3 Environment Institute, School of Earth & Environmental Sciences, University of Adelaide, Adelaide, South Australia, Australia, 4 Department of Conservation Biology,
Vegetation and Landscape Ecology, University of Vienna, Vienna, Austria, 5 Imperial College London, Ascot, Berkshire, United Kingdom, 6 The Bio-Protection Research
Centre, Lincoln University, Christchurch, New Zealand, 7 Technische Universität München, Department of Ecology and Ecosystem Management, Restoration Ecology,
Freising-Weihenstephan, Germany, 8 UFZ - Helmholtz Centre for Environmental Research, Department of Community Ecology, Halle, Germany, 9 German Centre for
Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany, 10 Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University,
Matieland, South Africa, 11 Institute of Botany, Department of Invasion Ecology, Academy of Sciences of the Czech Republic, Průhonice, Czech Republic, 12 Department
of Ecology, Faculty of Science, Charles University in Prague, Prague, Czech Republic, 13 Institute of Ecology and Evolution, University of Bern, Bern, Switzerland,
14 Environment Agency Austria, Department of Biodiversity and Nature Conservation, Vienna, Austria, 15 Redpath Museum, McGill University, Montreal, Quebec, Canada,
16 Estación Biológica de Doñana (EBD-CSIC), Seville, Spain, 17 South African National Biodiversity Institute, Kirstenbosch National Botanical Gardens, Claremont, South
Africa, 18 ISPRA, Institute for Environmental Protection and Research and Chair IUCN SSC Invasive Species Specialist Group, Rome, Italy, 19 Department of Biology, Unit
Ecology & Evolution, University of Fribourg, Fribourg, Switzerland
Abstract: Species moved by human
activities beyond the limits of their native
geographic ranges into areas in which they
do not naturally occur (termed aliens) can
cause a broad range of significant changes
to recipient ecosystems; however, their
impacts vary greatly across species and
the ecosystems into which they are introduced. There is therefore a critical need for a
standardised method to evaluate, compare,
and eventually predict the magnitudes of
these different impacts. Here, we propose a
straightforward system for classifying alien
species according to the magnitude of their
environmental impacts, based on the
mechanisms of impact used to code species
in the International Union for Conservation
of Nature (IUCN) Global Invasive Species
Database, which are presented here for the
first time. The classification system uses five
semi-quantitative scenarios describing impacts under each mechanism to assign
species to different levels of impact—
ranging from Minimal to Massive—with
assignment corresponding to the highest
level of deleterious impact associated with
any of the mechanisms. The scheme also
includes categories for species that are Not
Evaluated, have No Alien Population, or are
Data Deficient, and a method for assigning
uncertainty to all the classifications. We show
how this classification system is applicable
at different levels of ecological complexity
and different spatial and temporal scales,
and embraces existing impact metrics. In
fact, the scheme is analogous to the
already widely adopted and accepted
Red List approach to categorising extinction risk, and so could conceivably be
readily integrated with existing practices
and policies in many regions.
Introduction
Human activities are transforming natural environments by moving species
beyond the limits of their native geographic ranges into areas in which they do not
naturally occur. Many of these alien
species (Box 1) have caused substantial
changes to the recipient ecosystems. Such
changes have been measured by a burgeoning number of studies that consider a
Citation: Blackburn TM, Essl F, Evans T, Hulme PE, Jeschke JM, et al. (2014) A Unified Classification of Alien
Species Based on the Magnitude of their Environmental Impacts. PLoS Biol 12(5): e1001850. doi:10.1371/
journal.pbio.1001850
Published May 6, 2014
Copyright: ß 2014 Blackburn et al. This is an open-access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited.
Funding: The sDiv workshop that led to the sImpact working group was funded by the German Research
Foundation DFG (FZT 118). JP, PP, and ZM acknowledge the support from long-term research development
project no. RVO 67985939 (Academy of Sciences of the Czech Republic), Centre of Excellence PLADIAS no. 1436079G, and grant no. P504/11/1028 (Czech Science Foundation), and institutional resources of the Ministry of
Education, Youth and Sports of the Czech Republic. PP acknowledges the support by the Praemium Academiae
award from the Academy of Sciences of the Czech Republic. JMJ acknowledges support from the ERA-Net
BiodivERsA (project FFII), with the national funder German Research Foundation DFG (JE 288/7-1). SK
acknowledges financial support from the Swiss National Science Foundation, the DST-NRF Centre of Excellence
for Invasion Biology, and the Drakenstein Trust. DMR and JRUW acknowledge support from the DST-NRF Centre
of Excellence for Invasion Biology and the National Research Foundation (grants 85417 and 86894, respectively).
AS acknowledges financial support of the German Academic Exchange Service (DAAD). MV acknowledges
support from the Severo Ochoa Program for Centres of Excellence in R+D+I (SEV-2012-0262). The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Essays articulate a specific perspective on a topic of
broad interest to scientists.
Abbreviations: CG, cryptogenic; DD, Data Deficient; GISD, Global Invasive Species Database; IUCN,
International Union for Conservation of Nature; MA, Massive; MI, Minor; ML, Minimal; MO, Moderate; MR,
Major; NA, No Alien Population; NE, Not Evaluated; SSC, Species Survival Commission.
* E-mail: tim.blackburn@ioz.ac.uk
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broad range of environmental impacts,
defined here as measurable changes to the
properties of an ecosystem by an alien
species [1,2], at different levels of organisation (Box 1). For example, alien species
have been shown to cause significant
changes in native species extinction probabilities, genetic composition of native
populations, behaviour patterns, species
richness and abundance, phylogenetic and
taxonomic diversity, trophic networks,
ecosystem productivity, nutrient and contaminant cycling, hydrology, habitat structure, and various components of disturbance regimes [1–8]. Such changes are
often indirect, and may involve subtle or
poorly studied interactions that could yield
substantial effects over time [9]. For these
reasons, most scientists and conservation
organisations consider alien species to be
undesirable additions to ecosystems, and
frequently devote considerable resources
towards preventing or mitigating their
impacts.
However, many alien species apparently
have had little or no detectable effects on
their new environment [1,10,11], and
some effects may be considered to be
positive [12–16]. It has been further
claimed that alien species are no more
likely to have undesirable impacts than
natives, and therefore that management
attention should be based on impacting
species in general, rather than on the
alien/native origin of species [17,18],
although this view is controversial
[19,20]. These commentators urge conservationists and land managers to organise priorities around whether species are
producing net benefits or harm, so as
to avoid wasting valuable conservation
resources on the costs of excluding (e.g.,
through ballast-water treatment), eradicating, containing, or controlling alien species
[21]. Recognising that impacts vary greatly among species and among recipient
systems, and that many notable impacts
only become obvious or significantly
influential long after the onset of invasion,
a critical need for invasion biology is the
capacity to evaluate, compare, and predict
the magnitudes of the impacts of different
alien species, in order to determine and
prioritise appropriate actions where necessary. The challenge is how to compare
impacts attributable to diverse alien taxa
on different levels of ecological complexity
(individuals, populations, communities,
ecosystems), at different spatial and temporal scales, assessed using a range of
metrics and techniques [22].
In response to these issues, here we
propose a simple standardised system for
classifying alien species in terms of the
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magnitude of their impacts. Our aim is to
produce a practical tool to report on the
impacts caused by alien species, that can
(i) be used to identify those species that
have different levels of environmental
impact, (ii) facilitate comparisons of the
level of impact from alien species among
regions and taxa, (iii) facilitate predictions
of potential future impacts of the species
in the target region and elsewhere, (iv)
align with the mechanisms of impact
identified in the International Union for
Conservation of Nature (IUCN) Global Invasive Species Database ([GISD];
http://www.issg.org/database), and (v)
prioritise management actions. The system we propose has the following properties, many of which also underlie the
intentions of the IUCN Red List categories and criteria (our classification system
can be viewed as broadly analogous to
that approach) [23]:
of impact of an introduction, rather
than on the likelihood of an invasion.
7. Classification is based on the best available evidence. Hence, species can move
up and down impact categories as the
quality of evidence improves, as conditions change, or as an invasion proceeds.
8. The scheme we propose here can be
applied to impacts assessed at a range of
spatial scales, from global to national or
regional.
Classifying Impact
1. The classification considers only environmental (as opposed to economic or
societal) impacts (see Box 1 for definitions). Nevertheless, our scheme could be
extended to social and economic impacts,
as well as to environmental impacts on
resident alien species that are perceived to
be harmless or beneficial.
2. The classification identifies species that
have deleterious abiotic or biotic impacts
(Box 1). Its aim is not to weigh deleterious
against beneficial impacts to determine
the net value of an introduction, but
rather to highlight potential consequences.
3. Species are classified on the basis of
evidence of their most severe documented impacts in regions to which
they have been introduced. The scheme
is, therefore, not a predictive model
of impact—however, by reporting on
the worst observed case, it can be used
to flag species with high potential
impacts that need to be evaluated
in detail in a particular introduction
context.
4. The classification provides a consistent
procedure for translating the broad
range of impact types and measures into
ranked levels of environmental impact. It
therefore distinguishes between taxa with
different magnitudes of impact.
5. The classification can be applied across
taxa, so that different taxa can be
compared using a common currency in
terms of their environmental impact. It
could also be applied at different taxonomic levels.
6. The classification considers consequences, not likelihoods; that is, it
focuses on the consequences in terms
Our classification system is based on the
Generic Impact Scoring System (GISS) to
compare the impacts of alien animal
species among members of large taxonomic groups, developed by Nentwig and
colleagues [24] and subsequently extended
by Kumschick and colleagues [25], modified to align it to the new impact scheme
of the GISD implemented by the IUCN
Species Survival Commission (SSC) Invasive Species Specialist Group (Figure 1).
The extended GISS [25] identified a set
of six impact classes (herbivory; competition; predation; disease transmission; hybridisation; impact on ecosystem, other
than those mentioned before, i.e., chemical, physical, or structural changes), which
we here term impact mechanisms (Box 1).
Each of these mechanisms was associated
with one of a sequential series of six impact
scenarios (ranked 0–5) describing increasing levels of impact by aliens by that
mechanism. These semi-quantitative scenarios were designed such that each step
change in category reflects an increase in
the order of magnitude of the particular
impact so that a new level of organisation
is involved. Thus: (0) no discernible
impact; (1) discernible impacts, but no
effects on individual fitness; (2) effects on
fitness, but not on populations; (3) changes
to populations, but not to community
composition; (4) community changes,
which are reversible; and (5) irreversible
community changes and extinctions. Species impacts are assessed and assigned to a
scenario for each impact mechanism. The
scenario ranks assigned for each impact
mechanism can be summed to produce an
overall impact score. Species can then be
compared with respect to these scores, for
example to identify traits associated with
higher levels of impact [24,26].
Our classification scheme is based on the
impact mechanisms and scenarios presented by Kumschick and colleagues [25], but
modified in four ways. First, and most
importantly, we added new scenarios for
mechanisms of impact additionally identi-
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fied in the IUCN GISD. The GISD scheme
identifies 13 impact mechanisms (Figure 1),
along with associated outcomes of those
impacts in respect of changes to environmental or socio-economic parameters. Of
these, numbers 1–4 and 8 correspond
directly to scenarios in Kumschick and
colleagues [25], while mechanisms 9–11
are captured under Kumschick and colleague’s mechanism of impact on ecosystem (see above). We therefore expanded the
Kumschick and colleagues scheme by
adding explicit scenarios for four mechanisms of impact in the GISD schema:
parasitism (impact 5 in Figure 1), poisoning/toxicity (impact 6), bio-fouling (impact
7), and interaction with other invasive
species (impact 12). We ignored the thirteenth mechanism (other), as it is not
possible to derive scenarios for unspecific
impacts (although impacts not captured by
the first 12 mechanisms can still be assigned
on the basis of the general meanings
identified in Table 1).
Second, Kumschick and colleagues [25]
described scenarios of deleterious and
beneficial environmental impacts by alien
taxa, but here we consider only the
deleterious impacts (see point 2 above).
Third, we combined the two lowest
ranking scenarios for each mechanism.
The zero-ranked scenario in each case
always refers to ‘‘No impact known or
detectable,’’ but as the presence of an alien
individual in a new environment always
produces a change to the properties of an
ecosystem (e.g., by altering its genetic or
species diversity), by definition it has a
non-zero impact in some context. Note
that there is a crucial distinction between
species with no known impacts, and
species for which there is insufficient
evidence to assess impact (see section in
Box 2 on ‘‘Data Deficient’’ species).
Finally, we edited the scenarios of
Kumschick and colleagues [25] to resolve
some terminological ambiguities in respect
of our classifications, and to ensure that
the scenarios are aligned with the mechanisms of impact identified in the GISD.
Instead of using the impact mechanisms
and scenarios to produce an overall
Box 1. A Glossary of Key Definitions
Alien species: a species moved by human activities beyond the limits of its
native geographic range into an area in which it does not naturally occur. The
movement allows the species to overcome fundamental biogeographic barriers
to its natural dispersal. Common synonyms are exotic, introduced, nonindigenous, or non-native [50].
Environmental impact: a measurable change to the properties of an ecosystem
by an alien species [2]. Our definition means that our scheme applies to all
ecosystems—whether largely natural or largely managed by humans—but
explicitly considers only effects that have impacts on the native biota or the
ecosystem processes that derive from that environment. The same alien species
may also have impacts on human societies and economies [37], but these
represent additional and complex dimensions of impacts [51–56], and one should
avoid conflating environmental with non-environmental impacts.
Deleterious impact: an impact that changes the environment in such a way as
to reduce native biodiversity or alter ecosystem function to the detriment of the
incumbent native species—as indicated by a change in importance or abundance
following invasion. This is similar to the ‘‘adverse effect’’ concept [57]. This
definition intentionally excludes societal judgments regarding the desirability or
value of aliens, although our assumption is that the classification will be used as a
mechanism to prevent impacts that are judged to be ‘‘negative’’ by those
concerned.
Impact mechanisms: categories into which different types of alien species
impact are classified. The IUCN GISD identifies 13 such categories; a list of these
impact mechanisms is given in Figure 1.
Propagule pressure: a composite measure of the number of individuals that
are released or escape into a region to which they are not native. It incorporates
estimates of the absolute number of individuals involved in any one release/
escape event (propagule size) and the number of discrete such events (propagule
number) [58].
Residence time: the length of time that an alien species has been in its
introduced range [59].
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numerical impact score for a species, we
use the scenarios to assign a species to one
of five sequential categories of impact: in
ascending order of impact, these categories are Minimal (ML), Minor (MI),
Moderate (MO), Major (MR), and Massive (MA) (Figure 2; Box 2). The process of
categorisation would involve collation of
all available evidence on impact for the
members of a taxon from all regions to
which the taxa have been introduced (or
from the focal region where relevant), and
using that evidence to inform expert
opinion on the category of impact indicated. The impact category to which a
species is assigned is that corresponding to
the highest level of deleterious impact
identified from any of the impact mechanisms (Box 2; Table 1). Listing of a species
in a higher category explicitly assumes that
there is evidence that the species has had a
greater deleterious impact on some aspect
of an environment in which it is alien than
a species in a lower category of impact.
Impact rating should be considered in the
absence of management, but our approach
may contribute to a process of prioritising
species for management (e.g., if a new
incursion by a high impact species is
detected), as is required by Aichi target 9
of the Convention on Biological Diversity’s
Strategic Plan 2020 (www.cbd.int/sp/
targets/rationale/target-9). We would expect some species to move between categories in successive categorisation processes, at the most trivial level from Not
Evaluated (NE) into one of the evaluated
categories (Figure 2), but subsequently from
No Alien Population (NA) to an alien
category (Data Deficient [DD], or one of
Minimal (ML), Minor (MI), Moderate
(MO), Major (MR), or Massive (MA) if
introduced into the wild beyond its natural
range limits), and potentially then between
different categories of alien impact. Species
whose alien status is uncertain can be
identified as cryptogenic (CG) within any
of the impact categories (Box 2).
Uncertainty
There are likely to be many cases where
uncertainty exists about the correct categorisation of a species in terms of the
magnitude of its impacts, even for species
for which data is considered adequate (Box
2; Table 1). Consequently, it will be
sensible to include an estimate of the
degree of uncertainty attached to all
categorisations, so that the degree of
confidence in every classification is explicitly made clear. Only epistemic or reducible uncertainty (i.e., uncertainty due to
data quality) is of importance for the
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Figure 1. Impact scheme of the Global Invasive Species Database, implemented by the IUCN Species Survival Commission (SSC)
Invasive Species Specialist Group. The GISD stores detailed information on more than 800 invasive alien species, including on the impacts they
cause. The GISD has recently been redesigned, and all information has been re-classified in order to improve the searching functionalities of the
database. The schema developed for the revised GISD has allowed all species stored in the database to be coded in respect of the direct mechanisms
by which their impacts occur (e.g., predation), and by the outcomes of those impact mechanisms on the environment or on human activities. For
example, the grass Imperata cylindrica (Poales: Poaceae) almost doubles litter biomass in invaded locations, which increases potential fuel for fires
(impact mechanism coded as flammability, and impact outcome as modification of fire regime). The plant Schinus terebinthifolius (Sapindales:
Anacardiaceae) is a bio-fouling agent, forming dense thickets in gullies and river bottoms, with the ultimate effect of changing the hydrology of river
streams of invaded freshwater bodies (mechanism coded as bio-fouling, and impact outcome described as modification of hydrology). The insect
Adelges piceae (Hemiptera: Adelgidae) releases a toxin causing stress to trees, which eventually die. The impact outcome of A. piceae is described in
GISD as damage to forestry, with its mechanism of impact coded as poisoning/toxicity, but it can also be coded as having an environmental impact
on plant/animal health, as it has been here. In the table, mechanisms and outcomes are reported in two separate columns, and the three examples of
the connections between mechanisms and outcomes are shown. Impact outcomes in the GISD database can be environmental or socio-economic,
but our categorisation scheme of species in terms of the magnitudes of their impacts (Figure 2; Table 1) concerns only the former.
doi:10.1371/journal.pbio.1001850.g001
proposed classification. Uncertainty related to variation in impacts in space or time
(stochasticity or irreducible uncertainty) is
not considered because only the highest
impact reported is considered. We acknowledge that there are different ways to
characterise uncertainty, but we suggest
for practical purposes a categorisation of
uncertainty into three levels—high, medium, and low confidence—based on approaches used by the Intergovernmental
Panel on Climate Change (IPCC) [27] and
European and Mediterranean Plant
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Protection Organization (EPPO) [28,29].
Further details are given in Tables S1 and
S2 and Text S1.
What follows is a condensed version of
our Discussion for the general reader: we
encourage those with a more specific
interest in the subject to read the full
version, available as Text S2.
There are abundant examples of alien
species having deleterious environmental
impacts that alter the structure, function,
or dynamics of the ecosystem concerned.
The need to prioritise management responses to these impacts (or the objectively
quantified risk of such threats) provides a
strong impetus to develop a standardised
system by which impacts can be rigorously
quantified and compared in terms of their
magnitudes. However, there is no commonly employed method of quantifying
and ranking impacts on biodiversity and
ecosystems [30]. Regulatory bodies have
attempted to develop a variety of different
4
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Discussion
Table 1. Impact criteria for assigning alien species to different categories in the classification scheme (Box 2).
Impact Class
Massive (MA)
Major (MR)
Moderate (MO)
Minor (MI)
Minimal (ML)
Categories should
adhere to the
following general
meaning
Causes at least local
extinction of species,
and irreversible changes
in community composition;
even if the alien species is
removed the system does
not recover its original
state
Causes changes in
community composition,
which are reversible if the
alien species is removed
Causes declines in
population densities,
but no changes in
community composition
Causes reductions in
individual fitness, but no
declines in native population
densities
No effect on
fitness of
individuals of
native species
Competition (1)
Competition resulting
in replacement or local
extinction of one or
several native species;
changes in community
composition are
irreversible
Competition resulting in
local or population
extinction of at least one
native species, leading to
changes in community
composition, but changes
are reversible when the alien
species is removed
Competition resulting
in a decline of population
size of at least one native
species, but no changes in
community composition
Competition affects
fitness (e.g., growth,
reproduction, defence,
immunocompetence) of
native individuals without
decline of their populations
Negligible level
of competition
with native
species;
reduction of
fitness of native
individuals is
not detectable
Predation (2)
Predators directly or
indirectly (e.g., via
mesopredator release)
resulting in replacement
or local extinction of one
or several native species
(i.e., species vanish from
communities at sites
where they occurred
before the alien arrived);
changes in community
composition are
irreversible
Predators directly or
indirectly (e.g., via
mesopredator release)
resulting in local or
population extinction of at
least one native species,
leading to changes in
community composition, but
changes are reversible when
the alien species is removed
Predators directly or
indirectly (e.g., via
mesopredator release)
resulting in a decline of
population size of at least
one native species but no
changes in community
composition
Predators directly or
indirectly (e.g., via
mesopredator release)
affecting fitness (e.g.,
growth, reproduction)
of native individuals without
decline of their populations
Negligible level
of predation on
native species
Hybridisation (3)
Hybridisation between the
alien species and native
species is common in the
wild; hybrids are fully
vigorous and fertile; pure
native species cannot be
recovered by removing
the alien, resulting in
replacement or local
extinction of native
species by introgressive
hybridisation (genomic
extinction)
Hybridisation between
alien species and native
species is common in the
wild; F1 hybrids are vigorous
and fertile, however offspring
of F1 hybrids are weak and
sterile (hybrid breakdown),
thus limited gene flow
between alien and natives;
individuals of alien species
and hybrids discernible from
pure natives, pure native
populations can be recovered
by removing the alien and
hybrids.
Hybridisation between
alien species and native
species is regularly
observed in the wild;
hybrids are vigorous, but
sterile (reduced hybrid
fertility),limited gene flow
between alien and natives,
local decline of populations
of pure native species, but
pure native species persists
Hybridisation between
alien species and native
species is observed in the
wild, but rare; hybrids are
weak and never reach
maturity (reduced hybrid
viability), no decline of pure
native populations
No hybridisation
between alien
species and
native species
observed in the
wild (prezygotic
barriers),
hybridisation
with a native
species might
be possible in
captivity
Transmission of
diseases to native
species (4)
Transmission of diseases
to native species resulting
in replacement or local
extinction of native species
(i.e., species vanish from
communities at sites
where they occurred
before the alien arrived);
changes in community
composition are irreversible
Transmission of diseases
to native species resulting
in local or population
extinction of at least one
native species, leading to
changes in community
composition, but changes
are reversible when the alien
species is removed
Transmission of diseases
to native species resulting
in a decline of population
size of at least one native
species, but no changes in
community composition
Transmission of diseases
to native species affects
fitness (e.g., growth,
reproduction, defence,
immunocompetence)
of native individuals without
decline of their populations
The alien
species is not a
host of diseases
transmissible to
native species or
very low level of
transmission of
diseases to
native species;
reduction of
fitness of native
individuals is
not detectable
Parasitism (5)
Parasites or pathogens
directly or indirectly (e.g.,
apparent competition)
resulting in replacement or
local extinction of one or
several native species (i.e.,
species vanish from
communities at sites
where they occurred
before the alien arrived);
changes in community
composition are irreversible
Parasites or pathogens
directly or indirectly (e.g.,
apparent competition)
resulting in local or
population extinction of at
least one native species,
leading to changes in
community composition, but
changes are reversible when
the alien species is removed
Parasites or pathogens
directly or indirectly (e.g.,
apparent competition)
resulting in a decline of
population size of at least
one native species but no
changes in community
composition
Parasites or pathogens
directly or indirectly
(e.g., apparent competition)
affecting fitness
(e.g., growth, reproduction,
defence,
immunocompetence) of
native individuals without
decline of their populations
Negligible level
of parasitism or
disease
incidence
(pathogens) on
native species,
reduction of
fitness of native
individuals is
not detectable
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Table 1. Cont.
Impact Class
Massive (MA)
Major (MR)
Moderate (MO)
Minor (MI)
Minimal (ML)
Poisoning/
toxicity (6)
The alien species is toxic/
allergenic by ingestion,
inhalation, or contact to
wildlife or allelopathic to
plants, resulting in
replacement or local
extinction of native
species; changes in
community composition
are irreversible
The alien species
is toxic/allergenic by
ingestion, inhalation, or
contact to wildlife or
allelopathic to plants,
resulting in local or
population extinction
of at least one native
species (i.e., species
vanish from communities
at sites where they
occurred before the
alien arrived), leading to
changes in community
composition, but changes
are reversible when the
alien species is removed
The alien species
is toxic/allergenic
by ingestion, inhalation,
or contact to wildlife or
allelopathic to plants,
resulting in a decline
of population size of
at least one native
species, but no changes
in community
composition (native
species richness)
The alien species
is toxic/allergenic
by ingestion, inhalation,
or contact to wildlife
or allelopathic to
plants, affects fitness
(e.g., growth,
reproduction, defence,
immunocompetence)
of native individuals
without decline of
their populations
The alien
species is not
toxic/allergenic/
allelopathic, or if
it is, the level is
very low,
reduction of
fitness of native
individuals is
not detectable
Bio-fouling (7)
Bio-fouling resulting in
replacement or local
extinction of one or
several native species (i.e.,
species vanish from
communities at sites
where they occurred
before the alien
arrived); changes in
community composition
are irreversible
Bio-fouling resulting
in local or population
extinction of at least
one native species,
leading to changes
in community
composition, but
changes are reversible
when the alien species is
removed
Bio-fouling resulting
in a decline of
population size of
at least one native
species, but no
changes in community
composition
Bio-fouling affects
fitness (e.g., growth,
reproduction, defence,
immunocompetence)
of native individuals
without decline of their
populations
Negligible level
of bio-fouling
on native
species;
reduction of
fitness of native
individuals is
not detectable
Grazing/
herbivory/
browsing (8)
Herbivory resulting in
replacement or local
extinction of one or
several native plant
species (i.e., species
vanish from
communities at sites
where they occurred
before the alien
arrived); changes in
community composition
are irreversible
Herbivory resulting in
local or population
extinction of at least
one native plant species,
leading to changes in
community composition,
but changes are reversible
when the alien species is
removed
Herbivory resulting in a
decline of population
size of at least one native
species, but no changes in
community composition
Herbivory affects
fitness (e.g., growth,
reproduction, defence,
immunocompetence) of
individual native plants
without decline of their
populations
Negligible level
of herbivory on
native plant
species,
reduction of
fitness on native
plants is not
detectable
Chemical,
physical, or
structural
impact on
ecosystem (9,
10, 11)
Many changes in
chemical, physical,
and/or structural
biotope characteristics;
or changes in nutrient
and water cycling; or
disturbance regimes; or
changes in natural
succession, resulting in
replacement or local
extinction of native
species (i.e., species
vanish from communities
at sites where they
occurred before the
alien arrived); changes
(abiotic and biotic) are
irreversible
Changes in chemical,
physical, and/or
structural biotope
characteristics; or changes
in nutrient cycling; or
disturbance regimes; or
changes in natural
succession, resulting
in local extinction of
at least one native
species, leading to
changes in community
composition, but changes
are reversible when the
alien species is removed
Changes in chemical,
physical, and/or
structural biotope
characteristics; or
changes in nutrient
cycling; or disturbance
regimes; or changes
in natural succession,
resulting in a decline
of population size of
at least one native
species, but no
changes in community
composition
Changes in chemical,
physical, and/or
structural biotope
characteristics; or
changes in nutrient
cycling; or disturbance
regimes; or changes in
natural succession
detectable, affecting
fitness (e.g., growth,
reproduction, defence,
immunocompetence)
of native individuals
without decline of their
populations
No changes in
chemical,
physical, and/or
structural
biotope
characteristics;
or changes in
nutrient cycling;
or disturbance
regimes; or
changes in
natural
succession
detectable, or
changes are
small with no
reduction of
fitness of native
individuals
detectable
PLOS Biology | www.plosbiology.org
6
May 2014 | Volume 12 | Issue 5 | e1001850
Table 1. Cont.
Impact Class
Massive (MA)
Major (MR)
Interaction
with other alien
species (12)
Interaction of an
Interaction of an alien
alien species with
species with other
other aliens (e.g.,
aliens (e.g., pollination,
pollination, seed
seed dispersal, habitat
dispersal, habitat
modification) facilitates
modification) facilitates
local or population
replacement or local
extinction of at least
extinction of one or
one native species, and
several native species (i.e., produces changes in
species vanish from
community composition
communities at sites
that are reversible but would
where they occurred
not have occurred in the
before the alien arrived),
absence of the species.
and produces irreversible
These interactions may be
changes in community
included in other impact
composition that would
classes (e.g., predation,
not have occurred in the
apparent competition) but
absence of the species.
would not have resulted in
These interactions may be the particular level of impact
included in other impact
without an interaction with
classes (e.g., predation,
other alien species
apparent competition) but
would not have resulted in
the particular level of
impact without an interaction
with other alien species
Moderate (MO)
Minor (MI)
Minimal (ML)
Interaction of an alien
species with other aliens
(e.g., pollination, seed
dispersal, habitat
modification) facilitates a
decline of population
size of at least one native
species, but no changes in
community composition;
changes would not have
occurred in the absence
of the species. These
interactions may be
included in other impact
classes (e.g., predation,
apparent competition) but
would not have resulted
in the particular level of
impact without an
interaction with other alien
species
Interaction of an alien
species with other aliens
(e.g., pollination, seed
dispersal) affects fitness
(e.g., growth,
reproduction, defence,
immunocompetence) of
native species’ individuals
without decline of their
populations; changes
would not have occurred
in the absence of the
species. These interactions
may be included in other
impact classes (e.g.,
predation, apparent
competition) but would not
have resulted in the particular
level of impact without an
interaction with other alien
species
Interaction of an
alien species
with other aliens
(e.g., pollination,
seed dispersal)
but with
minimal effects
on native
species;
reduction of
fitness of native
individuals is
not detectable
These categories are for species that have been evaluated, have alien populations (i.e., are known to have been introduced outside their native range), and for which
there is adequate data to allow classification (see Figure 2). Classification follows the general principle outlined in the first row. However, we specifically outlined the
different mechanisms through which an alien species can cause impacts in order to help assessors to look at the different aspects and to identify potential research
gaps. Numbers next to different impact classes reference the numbering of impacts in the classification of impact mechanisms in the GISD (Figure 1).
doi:10.1371/journal.pbio.1001850.t001
schemes [31–33], but a unified standard
classification does not exist. Indeed, the
lack of a standard metric, coupled with
data deficiencies, is likely a major reason
why risk assessments rarely include quantitative evaluations of impact [34]. We
believe that our proposed classification
scheme (Figure 2; Table 1; Box 2) provides
a pragmatic solution to some of these
needs. It also has the attractive quality that
it follows a similar approach to the already
widely adopted Red Listing approach to
categorising extinction risk, and so could
theoretically be quickly integrated with
existing practices and policies across the
globe. It aligns with mechanisms of impact
identified in the IUCN GISD (Figure 1),
and hence can be used in conjunction with
that important database. The interlink
between the IUCN GISD and Red List
may also permit a more structured application of the present scheme to the
evaluation of the impact of alien species
on species assessed in the Red List.
Our scheme overcomes the problems
that arise from the fact that there is no
standard metric of impact, or method of
quantifying it. By relating quantitative
studies to a set of standardised semiquantitative scenarios enhanced by descriptions, we can identify and rank
PLOS Biology | www.plosbiology.org
mechanisms of impact indicated by the
evidence provided. Although there is often
a significant degree of uncertainty surrounding the impact of any given alien
species, both because of measurement
error and subsequent translation of what
a quantitative trait measure means in
terms of actual environmental change,
the broad separation of our categories in
terms of the level of impact they represent
means that impacts can be classified with a
good degree of confidence [24]. Furthermore, our scheme includes a mechanism
for appending estimates of uncertainty to
each categorisation (Text S1). Similar
issues of uncertainty pertain to the IUCN
Red List criteria and categories (albeit that
they are often overlooked), but while the
precise categorisation of some species is
the subject of considerable debate [35],
there is little doubt that the Red List
functions as an effective and credible guide
to the threat of extinction and as a
valuable trend indicator over time [36].
We hope that our categorisation scheme
will come to be viewed in the same light.
In contrast to the previous use of such
scenarios to estimate overall impact
[24,26,37], here they are simply used to
identify the mechanism by which a species
has its highest impact. A lack of data on
some mechanisms can affect estimates of
overall impact, but does not prevent the
classification of a species under our
scheme, if information is available on
other mechanisms of impact. Our categorisation scheme is therefore effective
with less available data than required to
assess the overall impact of a species.
A lack of information on some mechanisms of impact may lead to a species
being placed in a lower impact category
than might otherwise be the case. However, in many cases, it will be difficult to
distinguish whether an alien is the driver
of environmental changes, or simply a
‘‘passenger’’ responding to the same driver
as the natives [38]. Synergistic interactions
between alien species and other stressors
are also possible—and perhaps increasingly common—but difficult to anticipate
[39]. This suggests that categorisation will
be cautious: an alien is likely to be assigned
to a high impact category if it is associated
with significant change, even if it is not the
main driver. This is a sensible situation
under the precautionary principle, where
benefit of the doubt should not be given to
the alien. However, our system is intended
to be dynamic, allowing for updates as
new or more reliable data become available, and as the documented impact
7
May 2014 | Volume 12 | Issue 5 | e1001850
Box 2. Description of the Categories in the Impact Classification
Scheme
The relationship between categories is shown in Figure 2. A species is considered to
have a given level of impact (MA, MR, MO, MI, or ML) when the best available
evidence indicates that it has previously had impacts in a region to which it is not native
that meet any of the relevant criteria presented in Table 1. Species are categorised by
the most severe impact recorded under any impact mechanism (Table 1), as follows:
Massive (MA) A species is considered to have Massive impacts when it leads to the
replacement and local extinction of native species, and produces irreversible changes in the
structure of communities and the abiotic or biotic composition of ecosystems. Note that
‘‘local’’ refers to the typical spatial extent over which the original native communities can
be characterised.
Major (MR) A species is considered to have Major impacts when it causes the local
or population extinction of at least one native species, and leads to reversible changes in
the structure of communities and the abiotic or biotic composition of ecosystems, and has
no impacts that cause it to be classified in the MA impact category.
Moderate (MO) A species is considered to have Moderate impacts when it
causes declines in the population densities of native species, but no changes to the
structure of communities or to the abiotic or biotic composition of ecosystems, and
has no impacts that would cause it to be classified in a higher impact category.
Minor (MI) A species is considered to have Minor impacts when it causes reductions
in the fitness of individuals in the native biota, but no declines in native population densities,
and has no impacts that would cause it to be classified in a higher impact category.
Minimal (ML) A species is considered to have Minimal impacts when it is unlikely
to have caused deleterious impacts on the native biota or abiotic environment. Species
that have been evaluated under the categorisation process but for which impacts
have not been assessed in any study should not be classified in this category, but
rather should be categorised as Data Deficient.
Data Deficient (DD) A species is categorised as Data Deficient when the best
available evidence indicates that it has individuals existing in a wild state in a
region beyond the boundary of its native geographic range, but either there is
inadequate information to classify the species with respect to its impact, or
insufficient time has elapsed since introduction for impacts to have become
apparent. It is expected that all introduced species will have an impact at some
level, because by definition an alien individual in a new environment has a nonzero impact. However, listing a species as Data Deficient recognises that current
information is insufficient to assess that level of impact.
No Alien Populations (NA) A species is categorised as No Alien Populations
when there is no reliable evidence that it has or had individuals existing in a wild
state in a region beyond the boundary of its native geographic range. We assume
that absence of evidence is evidence of absence in this case, as it is impossible to
prove that a species has no alien individuals anywhere in the world. Species with
individuals kept in captivity or cultivation in an area to which it is not native [60]
would be classified here. A species could currently have no individuals existing in
a wild state in a region beyond the boundary of its native geographic range
because it has died out in, or has been eradicated from, such an area. In these
cases, there should be evidence relating to impact that causes it to be classified in
one of the impact categories (ML, MI, MO, MR, MA), or alternatively no evidence
of impact, which would cause it to be classified as Data Deficient.
Not Evaluated (NE) A species is Not Evaluated when it has not yet been
evaluated against the criteria, as is also the case in the IUCN Red List [23].
Cryptogenic (CG) Cryptogenic is not a category within the scheme presented
in Figure 2, but rather a label to be applied to those taxa for which it is unclear,
following evaluation, whether the individuals present at a location are native or
alien [61]. This is a particular problem in the marine realm, for cosmopolitan
plants and for many stored product arthropod pests, for which the native
geographic ranges are unknown. Cryptogenic taxa may have deleterious impacts
where they occur [62,63]. We suggest on the basis of the precautionary principle
that cryptogenic species are evaluated as if they were aliens, but that their impact
categorisation is modified by the CG label (e.g., for a cryptogenic species with
Major impact: Genus species MR [CG]).
PLOS Biology | www.plosbiology.org
8
history of a species unfolds through
space and time [40–42]. In fact, the classification scheme could in practice serve
to identify knowledge gaps for invaders
for which there is currently little or no
information.
The use of standardised scenarios allows
analysis of a wide range of factors relating
to impact, such as correlates of magnitude,
variation, and temporal and spatial
change. The category of impact to which
an alien species is assigned can increase or
decrease as more deleterious impacts are
discovered, if the alien species is subsequently identified as a passenger rather
than a driver of change, or if environmental influences change. The protocol can
also be applied with minor modification to
impacts at a range of spatial scales,
allowing national, regional, and global
categorisation of impacts. It complements
and can inform national assessment
schemes in which species are assigned to
different lists [43–45] depending on
whether they are species with a low risk
of impact (‘‘white list,’’ ML, or perhaps MI
in this scheme), of assumed or uncertain
impact (‘‘grey list’’), or have measurable
impacts of concern (‘‘black list,’’ corresponding to MO, MR, or MA) on
environments. In all of these respects, the
scheme is analogous to the IUCN Red List
[46]. Another similarity with the IUCN
Red List approach is that some impact
listings, as with some threat listings, are
likely to be context dependent. For
example, a relatively widespread taxon
may be classified as at high risk of
extinction in some national Red Lists if
the species is locally rare or threatened
(e.g., the country is near the range edge).
Similarly, an alien impact that is observed
in one area of the introduced range may
not occur elsewhere, or may not be as
important elsewhere: invasiveness, and by
extension impact, is a characteristic of a
population rather than a species [2,47].
Overall, the assessment of impacts at more
restricted scales may predominantly depend on evidence of impacts elsewhere
(which may be subject to higher error,
given context-dependent variation), whereas at large scales, information on impacts
will increasingly derive from the focal
region.
All of this highlights the importance of
ensuring that the impacts of aliens on populations and communities are measured at
an appropriate spatial scale, taking into
account the typical spatial size at which
original native communities can be characterised (termed the ‘‘local scale’’ here).
Studies at very restricted spatial scales (i.e.,
patches of 10s or 100s of square metres)
May 2014 | Volume 12 | Issue 5 | e1001850
Figure 2. The different categories in the alien species impact scheme, and the relationship between them. Descriptions of the
categories are provided in Box 2. The CG category is not represented in this diagram as CG taxa may be found in any category.
doi:10.1371/journal.pbio.1001850.g002
might overestimate impacts if extrapolated
to larger scales, while studies at extensive
spatial scales (i.e., regional or national)
might underestimate them. For example,
an alien species might be shown in a field
experiment to exclude natives from areas
the size of experimental plots, and perhaps
even to extirpate natives from entire habitat
patches, without having a significant effect
on community diversity (e.g., because of the
influence of spatial dynamics, refugia, or
rescue effects). In this case, it is likely that
populations of some natives would have
declined (e.g., competitors or food species)
in the habitats in which the alien species
occurs, without resulting in local extinctions: the appropriate classification under
our scheme would therefore be MO in
this case (Table 1). This approach has the
benefit of identifying impacts demonstrated in very small habitat patches that
PLOS Biology | www.plosbiology.org
may be a cause for greater concern in the
future.
One shortcoming of the proposed
classification scheme is that it is not
designed to be predictive by itself. For
example, it cannot be applied to species
with no previous history of alien populations (if evaluated, these species cannot
be classified other than NA), and, as
recorded impacts usually accrue with
population growth, species that have
not been introduced for long (short
residence times; Box 1) or not introduced
in large numbers (low propagule pressures; Box 1) are likely to receive a low
rating. Nevertheless, the scheme could
provide predictive information on the
likely magnitude of impacts of a species,
if it is phylogenetically or functionally
similar to a species that has known
impacts as an alien on the native biota
or abiotic environment [33], or if there is
a mechanistic understanding of how
impacts might progress. This may be
helpful given that a history of impact
elsewhere is currently often considered to
be the best available predictor of the
impact potential of an alien species
[40,48,49], but is of no use for predicting
impacts of species with no alien populations. Such species could be assessed
under our scheme, but with their categorisation assigned a high level of
uncertainty. We do not advocate that
such approaches substitute for the precautionary principle in cases of species
with unknown impacts, but they may
nevertheless help to understand which
species may be most damaging if introduced. A future development of the
scheme would be to include an estimate
of potential impact for such species.
9
May 2014 | Volume 12 | Issue 5 | e1001850
Supporting Information
Figure S1 The relationship between
the overall potential environmental
impact score and the impact category to which the species is assigned under our classification
scheme, for data on alien mammals
in Europe (from [9]). Environmental
impact score is the sum of the impacts
over the six categories given by
Kumschick and colleagues (39). Species
are assigned to impact category on the
basis of the largest impact value in any of
the six categories. Note that Kumschick
and colleagues (39) do not score impacts
under several of the classes listed in
Table 1. The analysis is confined to
impacts recorded for species in their alien
ranges in Europe (indicating the scalable
nature of our approach): a global analysis
might shift some species to higher impact
categories. Note that the data points have
been jittered to improve visibility. Impact
score and category are clearly positively
related, but some species can have higher
scores than other species in higher
categories.
(TIF)
Figure S2 Relationship between the
overall environmental impact of
European alien plants (the median
score across all assessed classes of
impact. Note that not all classes of
impact in Table 1 were assessed)
and the impact classification assigned under our scheme (defined
by the highest score achieved in
any of the impact classes). Species
with names indicated have, compared to
their average impact across the classes
assessed, a disproportionally strong impact in one individual class. While their
high impact may be overlooked when
assessing the overall impact, it is captured by our suggested classification
scheme under which species are assigned on the basis of maximum, not
average, impact. For example, Cortaderia
selloana exerts a strong impact (MA) on
ecosystem processes, its impacts in other
classes being MO at most. Note that
data points have been jittered to improve visibility. Based on M. Vilà, Z.
Marková, P. Pyšek, J. Pergl (unpublished data) following the impact assessment methodology of [10].
(TIF)
Table S1 Guidance regarding the
use of the confidence rating (modified from the EPPO pest risk as-
sessment decision support scheme
[2,64]).
(DOCX)
Table S2 Suggested distribution of
likelihoods (in percent) of the impact of alien species being in a
certain category depending on the
confidence of the assessment. Probability distributions follow a standardised
beta distribution with parameters a and b.
The histogram below the table provides a
pictorial representation of the same probabilities.
(DOCX)
Text S1
Categorising uncertainty.
(DOCX)
Text S2
Full version of the Discus-
sion.
(DOCX)
Acknowledgments
This study is a joint effort of the working group
sImpact that formed at a workshop at sDiv, the
Synthesis Centre within the German Centre for
Integrative Biodiversity Research (iDiv) HalleJena-Leipzig. We thank Ben Collen and Christian Lexer for comments that improved the
manuscript.
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May 2014 | Volume 12 | Issue 5 | e1001850